Abstract: Vascular diseases in birds are not uncommon, according to
findings from postmortem surveys. Although atherosclerosis affecting
psittacine birds appears overrepresented, some degenerative, infectious,
neoplastic, and congenital vascular diseases may also occur. A variety
of imaging diagnostic tools may be used to evaluate the avian vascular
system, such as conventional radiography, fluoroscopy, rigid endoscopy,
computed tomography, angiography, transcoelomic, and transesophageal
ultrasound examination. The wide array of current diagnostic imaging
tools offers the clinician capabilities to investigate avian
cardiovascular abnormalities. Further research in this domain and
constant efforts to apply several, and newer, vascular imaging
modalities in clinical cases are needed to expand our avian
cardiovascular knowledge base. The ability to diagnose vascular
pathologic processes in small avian patients may be improved by recent
developments in diagnostic imaging technology.

Cardiovascular diseases are common in avian species. (1-5)
Diagnostic imaging of the cardiovascular system is complicated by the
small size of the patients, the fast heart rates of birds, the presence
of air sacs, and the presence of the keel bone. The recognition of a
high incidence of atherosclerosis in birds (1,2,6,7) has generated an
interest in developing imaging modalities that will help identify
lesions antemortem. Techniques have been developed to image the avian
heart, but avian vascular imaging, itself, is still in its infancy. This
article reviews the vascular diseases that have been documented in birds
and the diagnostic imaging techniques that have been investigated in
these species. We hope to stimulate the much-needed research in this
field to develop current and future applications of avian vascular
imaging modalities.

Avian vascular diseases

Although birds may present with a variety of vascular conditions,
atherosclerosis is the most common vascular disease encountered in birds
from various orders (ie, Psittaciformes, Accipitriformes, Falconiformes,
Coraciiformes, Bucerotiformes, Struthioniformes, Galliformes, and
Columbiformes). (5) Atherosclerosis is characterized by calcification,
lipid retention, proteolytic injury, and a chronic inflammatory response
of the arterial wall, resulting in a loss of arterial elasticity, a risk
of atherosclerotic plaque rupture, or a narrowing of the vessel lumen.
(1,8) The disease is well described in captive birds and has
similarities to human atherosclerosis in that it is more prevalent in
aging individuals fed an unbalanced diet. (1) Atherosclerosis has been
reported in many birds in the Psittaciformes order, including Amazon
parrots (Amazona species), African grey parrots (Psittacus erithacus),
macaws (Ara species), and cockatoos (Cacatua species). (1) Anecdotally,
the disease was diagnosed in several avian species that were maintained
in zoological collections. (4,5,7) In psittaciform species, the reported
incidence of atherosclerosis from recent postmortem surveys (2,6,9,10)
varies between 4.6% to 91%. In pathologic studies of psittacine birds in
Europe, a high incidence of atherosclerosis has been reported, with an
approximately 91% incidence in African grey and Amazon parrots in one
study and 13% in psittacine birds in another study. (2,6) This contrasts
with the reported incidence in North America of 4.6% and lower. (7,10)
These differences may be the result of different environmental and
nutritional factors as well as different histopathologic criteria. In
one study, (7) atherosclerosis was considered significant enough to be
the cause of death in 26% of the affected birds. In birds submitted for
necropsy from a zoologic collection, 13.3% of birds with cardiovascular
lesions had evidence of atherosclerosis. (4) Additionally, cardiac
complications, such as congestive heart failure, are frequently reported
in clinical cases of atherosclerosis involving avian species. (11-15)
Several avian models have also been used to investigate cardiovascular
disease, including Japanese quail (Coturnix japonica), pigeons (Columba
livia), chickens, and turkeys. (16) Birds develop a central form of
atherosclerosis, with the great vessels at the base of the heart being
the primary site of pathologic lesions. (1,5,9) Atherosclerosis of the
coronary, carotid, and other peripheral arteries has rarely been
documented in avian species. (17-19)

Among other vascular diseases reported in birds, arterial aneurysm,
which may be described as a focal, blood-filled dilation of the arterial
wall communicating with the arterial lumen, has been documented in
various locations. The underlying cause of arterial aneurysms may be a
weakened arterial wall or a local disruption of the artery of origin,
which in either case may rupture. (20,21) Examples of aneurysms
diagnosed in avian species include a coronary aneurysm identified in an
umbrella cockatoo (Cacatua alba), (18) which apparently developed
secondary to atherosclerosis, and a mycotic aortic aneurysm in a wild,
female eider duck (Somateria mollissima). (22) Aortic aneurysms are also
found occasionally in poultry, specifically chickens and turkeys, and
anecdotally in ostriches (Struthio camelus). (21,23) In turkeys, aortic
aneurysms may develop as a consequence of aortic atherosclerosis leading
to aortic dissection. (24) Copper deficiency has also been suggested as
a cause of dissecting aneurysm and is considered rare in birds other
than turkeys. (21,23)

Acute ischemic stroke is occasionally seen in parrots. (19) Causes
are uncertain but atherosclerosis, arterial thromboembolism, or systemic
hypertension, as seen in humans, are suspected. One case (25) was
reported in a yellow-naped Amazon parrot (Amazona auropalliata) and was
associated with cerebral hemorrhage diagnosed by computed tomography
(CT) scan. Another case (26) was diagnosed and followed by serial
magnetic resonance imaging (MRI) in an African grey parrot.

Vasculitis is relatively uncommon in birds and is usually
associated with a systemic, infectious process. Vasculitis has
occasionally been reported, with Mycobacterium species and Aspergillus
species being identified as the underlying etiologic organisms. (21)
Mycobacterial granulomatous arteritis is infrequent and has been
diagnosed as primarily affecting the major and coronary arteries in 6
psittacine birds (budgerigar [Melopsittacus undulatus], cockatiel
[Nymphicus hollandicus], Moluccan cockatoo [Cacatua moluccensis],
grey-cheek parakeet [Brotogeris pyrrhopterus], white-capped pionus
[Pionus senilis], and rosella [Platycercus species]). (27) Aspergillus
species often colonize the vasculature adjacent to air sac lesions,
which may lead to thrombosis and emboli. (21) Filarioid worms have also
been described in the great vessels, particularly in the pulmonary
arteries and aorta, of various avian species. These include filaria of
the genus Splendidofilaria (Anatidae, American crow [Corvus
brachyrhynchos]; black-billed magpie [Pica pica]; and house sparrow
[Passer domesticus]), Sarconema (Anatidae), Paronchocerca (Ciconiidae,
Odontophoridae), Cardiofilaria (Cacatuidae, birds of prey), and
Chandlerella (Cacatuidae, Corvidae). (28)

Vascular tumors are relatively rare in birds. Although hemangiomas
and hemangiosarcoma are more common in their cutaneous form, they can
also develop on the main arteries. A hemangiosarcoma arising from the
right internal carotid was diagnosed in a double yellow-headed Amazon
parrot (Amazona ochrocephala oratrix). (29) A retrovirus, the avian
hemangioma virus, has been reported to induce multifocal vascular tumors
in chickens. (30)

Reports of congenital vascular diseases are scarce in birds. A
ventricular septal defect, diagnosed in an umbrella cockatoo and in a
Moluccan cockatoo, was associated with persistent truncus arteriosus in
the first case and with aortic hypoplasia in the second. (31) In these 2
cases, the diagnosis was obtained by transcoelomic echocardiography and
confirmed at necropsy.

Ventricular septal defects have also been documented in chickens,
turkeys, and in a tundra swan (Cygnus columbianus). (32-34)

[FIGURE 1 OMITTED]

Other vascular diseases that may have significant health
implications, but are poorly characterized in birds, are systemic
hypertension and arterial thromboembolism.

Diagnosis of vascular diseases

Currently, little information is available regarding the diagnosis,
treatment, and management of avian vascular diseases. Specifically, the
diagnosis of atherosclerosis remains challenging. Antemortem diagnosis
of atherosclerosis is primarily obtained in advanced cases, with severe
calcification of the arteries, or in association with congestive heart
failure. (11,14,35) A better knowledge and use of current and advanced
imaging techniques to assess avian blood vessels may help in early
diagnosis of avian vasculopathy in general and atherosclerosis in
particular.

[FIGURE 2 OMITTED]

Vascular diseases target the major arteries in birds and,
fortunately, these arteries are the most accessible to diagnostic
imaging. The blood vessels that are readily visible on imaging include
the 2 brachiocephalic trunks, which are the largest arteries in most
birds; the ascending aorta, which arises from the right brachiocephalic
trunk; the abdominal aorta; the 2 pulmonary arteries and veins; and the
2 carotid arteries that start from the brachiocephalic trunks (Fig 1).
Occasionally, the jugular veins, cranial and caudal vena cava,
mesenteric artery, and some visceral arteries may also be visualized.

Radiography: Radiographs are often one of the first diagnostic
tests performed in the avian patient. The central arteries can usually
be well visualized and delineated (Figs 2 and 3). The brachiocephalic
trunks, aorta, pulmonary arteries, and the pulmonary veins can usually
be localized. On the ventrodorsal view, the ascending aorta can be
visualized on the right of the midline (Fig 3). Central vessels are more
conspicuous in large birds and in birds with hyperinflated air sacs.
Radiographs are a relatively insensitive method of detecting vascular
diseases, but significant calcification of the great vessels is
occasionally present with atherosclerosis and is fairly specific for
this disease. (11) Despite the lack of objectivity, the major arteries
may appear prominent on radiographs with central atherosclerosis. (36) A
case of mycotic aneurysm in an eider (22) and another of vascular
neoplasia in a double yellow-headed Amazon parrot (29) appeared as
large, soft tissue opacities on the right side of the heart. Although
nonspecific, secondary cardiomegaly may be seen in birds with
atherosclerosis. (13,14)

[FIGURE 3 OMITTED]

Fluoroscopic angiography: Fluoroscopic angiography can visualize
the heart and vascular tree in real time. Under general anesthesia, the
bird is initially positioned in left lateral recumbency on a fluoroscopy
table. A bolus of nonionic iodinated contrast agent (2 mL/kg IV; iohexol
240 mg/mL; Omnipaque, GE Healthcare Inc, Princeton, NJ, USA) is
injected, at a rate of 1-2 mL/kg per second, through a catheter inserted
into the basilic or medial metatarsal vein during video acquisition at a
rate of 30 frames/s for the best resolution. The same bolus is repeated
to obtain the ventrodorsal view with the bird placed in dorsal
recumbency. The brachiocephalic trunks, aorta, pulmonary arteries,
pulmonary veins, and caudal vena cava can be seen (Fig 4). The
brachiocephalic trunks and aorta can be seen pulsating with the
heartbeats. Marked lumen changes can be observed during the cardiac
cycle. The procedure is easy and inexpensive and can be recorded for
further analysis and measurements. For measurement, to account for
different degrees of magnification, a calibrated marker should be kept
in the field during fluoroscopic acquisition.

[FIGURE 4 OMITTED]

Digital subtraction angiography is a fluoroscopic technique used in
interventional radiology to clearly visualize blood vessels in a dense
soft tissue or bone environment. Images are produced by subtracting a
precontrast image from later images once the contrast medium has been
introduced into the vascular system, which results in visualizing only
the contrast-filled vessels, without the background. It considerably
increases the outlines of the arteries and the detection of smaller
arteries not seen with conventional angiography, specifically for
extremities, such as legs, wings, and the head, but the images tend to
be easily degraded by small motions and noise (Fig 5) (H. B. and R. P.,
unpublished data, November 2009). A preliminary, nonenhanced
fluoroscopic image is recorded before administering a bolus of contrast
medium and is digitally subtracted during the angiography procedure. The
same bolus technique and a similar dose of contrast medium as used for
regular fluoroscopic angiography are used for digital subtraction
angiography, except that this option is selected in the machine. Reports
of angiography applications are still limited in birds. A coronary
aneurysm was diagnosed with angiography in an umbrella cockatoo. (18)
Angiocardiography has also been used clinically in a racing pigeon, 2
blue and gold macaws (Ara ararauna), and a whooper swan (Cygnus cygnus).
(13,36,37)

[FIGURE 5 OMITTED]

Ultrasonography: Echocardiography is, to date, the most useful
diagnostic test in avian cardiology. Well-established protocols have
been published for transcoelomic and transesophageal echocardiography.
(38-41) Images are typically acquired with an 8-11 MHz phased-array
transducer. The base of the aorta and the aortic valves can be imaged
via the vertical view in transcoelomic echocardiography but the
resolution is often poor (Fig 6). Nevertheless, reference ranges for the
aortic root diameter have been reported. (39-41) The aortic outflow
velocity has also been investigated, and reference ranges have been
provided for several psittacine birds and raptorial species. (39,40,42)
Transesophageal echocardiography presents an alternative to the
transcoelomic approach and offers greater details and the possibility of
performing an M-mode examination of the left ventricle and the aortic
root (Fig 7). The transverse and longitudinal views, with the
transesophageal echocardiography probe placed in a cranial position,
provide adequate details of the aortic root in most species. (38)
Contrast echocardiography has been evaluated in several avian species
(H. B. and R. P., unpublished data, November 2009). Ultrasound contrast,
consisting of perflutren lipid microspheres (Definity, Lantheus Medical
Imaging Inc, North Billerica, MA, USA), can be injected slowly, at a
dose of 0.1 mL/bird IV, after the contrast is shaken with a mechanical
activating device (Vialmix, Lantheus Medical Imaging) following
manufacturer recommendations. During imaging, a low acoustic power
(mechanical index, 0.2-0.3) should be used to prevent disruption of the
intravascular microspheres. The small size of the microspheres allows
them to go through the pulmonary capillary bed and they can consequently
be visualized in the left cardiac chambers. This is an advantage over
the injection of a small volume of agitated saline, which only opacities
the right cardiac chambers but can also reveal intracardiac and
extracardiac right to left shunts. The addition of contrast may help
better delineate the endocardial border of the left ventricle and
provide more accurate measurements of the diastolic and systolic
ventricular internal diameter and aortic root. The contrast is slowly
injected via a peripheral catheter while the heart is imaged with
transcoelomic or transesophageal echocardiography. The contrast lasts
several minutes, and the microspheres can be destroyed by increasing the
acoustic power if deemed necessary. No adverse effects have been noticed
with the use of perflutren in the birds imaged.

[FIGURE 6 OMITTED]

[FIGURE 7 OMITTED]

Endoscopy: Several endoscopic approaches can provide impressive
visualization of several arteries. The standard left and right lateral
approaches (43,44) lead to the visualization of the vessels supplying
the abdominal organs in the abdominal air sacs, such as the abdominal
aorta, iliac arteries, mesenteric artery, renal arteries, the caudal
vena cava, and the ischiatic veins (Fig 8). Additionally, the pulmonary
arteries and veins can be seen close to the base of the heart in the
left and right cranial thoracic air sacs (Fig 9). The least commonly
used interclavicular approach (43,44) provides access to the base of the
heart in the interclavicular air sac and should be considered the
approach of choice to evaluate the great arteries, carotid arteries, and
base of the heart. At this site, all the major and cranial arteries,
such as the brachiocephalic trunks, the ascending aorta, the brachial
arteries, the carotid arteries, the pulmonary arteries, and the jugular
veins, can easily be identified (Figs 10 through 12). Accumulation of
fat at the base of the heart can significantly impair the visualization
of the arteries through the interclavicular approach. There is a report
(29) of a hemangiosarcoma arising from the right carotid artery that was
diagnosed with the help of endoscopy in a double yellow-headed Amazon
parrot.

CT angiography: A CT examination provides an excellent assessment
of all major arteries and their anatomy in psittacine and raptorial
birds. The addition of contrast media greatly enhances the visualization
of the arteries and veins and their lumen. The patient should be
anesthetized for intravenous catheter placement and contrast
administration. We suggest first performing a whole body scout in
orthogonal planes, followed

by a survey precontrast examination with a built-in abdominal scan
protocol and the following parameters: standard algorithm in helical
scan mode, 1.25-mm slice thickness, 1.375 pitch, 100 kilovolt (peak),
and 150 mA. A dynamic, axial CT scan is recommended on a predetermined
slice with a single initial bolus of iohexol, 1 mL/kg given over 1
second. The starting time of the dynamic scan must coincide with the
initiation of the contrast administration. Dynamic scans allow the time
of arrival of the contrast medium (time to enhancement peak) at the
aorta or other selected artery to be determined. The CT angiography
(CTA) is then performed by the same scan parameters as the survey
precontrast series with 3 mL/kg of contrast media administered over 3
seconds. When performing the angiographic portion of the series, the
start of the contrast administration should preceed the start of
scanning by the time to the enhancement peak previously determined by
the dynamic axial CT. (45) Additional reconstruction series with thinner
slices (eg, 0.625 mm) and a soft tissue algorithm are recommended.

[FIGURE 8 OMITTED]

[FIGURE 9 OMITTED]

[FIGURE 10 OMITTED]

[FIGURE 11 OMITTED]

[FIGURE 12 OMITTED]

An injection pump may be used, but it can be problematic with the
small injection volume required in birds, and we prefer manual
injection. In small to medium sized birds, because of their fast
circulation of contrast in the vascular tree, the time to enhancement
peak in the aorta is very fast, and it is recommended that the CTA scan
be performed immediately after administration of the contrast. (45)
Reference ranges have been published (45) for arterial diameters of the
brachiocephalic trunks, ascending aorta, abdominal aorta, and pulmonary
arteries (Fig 13). The use of a mediastinal window or a manual
angiography window is recommended for more accurate and repeatable
measurements. A previously described (45) technique was performed with a
16-slice, multidetector CT; and the exact timing for injection and
acquisition of images recommended for CT machines that are not 16-slice
will likely vary, as will the resolution of the image.

Computed tomography angiography also allows the caudal and cranial
vena cava (Fig 14), the carotid arteries, the mesenteric artery and some
of its ramifications, and several of the smaller arteries of the avian
body to be visualized. In addition, 3-dimensional reformatting and
segmentation on the heart and central arteries are possible and may help
in the diagnosis of aneurysm and congenital vascular anomalies (Fig 15).
Although no case report, to our knowledge, documents the use of CTA in a
clinical context in birds, its use may prove to be invaluable in
assessing arterial luminal stenosis, aneurysm, dilatation of the
arteries, and calcification of the walls. In humans, CTA remains one of
the preferred methods for measuring arterial diameters, and multiple
studies have investigated its accuracy. (46-49) High-resolution CTA has
also been used in birds to describe normal vascular anatomy. (50)

Magnetic resonance imaging: Magnetic resonance angiography has not
been investigated in birds so far. In a study on MRI in healthy pigeons,
the hepatic and renal vasculature were discernable. (51) However, motion
artifacts prevented adequate imaging of the heart. Additionally, MRI was
not of good diagnostic value for the vascular system because of the fast
circulation of contrast media (gadolinium) through the vasculature and
the small size of the vessels to be investigated. To achieve a
diagnostic quality image in such small vessels, higher magnetic fields
would be required (3 T or higher), which further limits its clinical
use.

Conclusion

A variety of imaging modalities are available for the avian
vascular system. These techniques are presently underused, despite a
significant incidence of atherosclerosis in the captive bird population.
Angiography by fluoroscopy and CT scan may become the diagnostic tests
of choice to better characterize gross vascular lesions. Endoscopy by
the interclavicular approach allows direct visualization of the great
arteries but is more invasive and may be impaired by fat stores in
overweight animals. More studies and clinical reports are needed to
document the usefulness of vascular diagnostic imaging in birds. As
avian vascular imaging finds inspiration and application from human
cardiovascular imaging and pediatric cardiology, the span of diagnostic
tests and clinical applications will undoubtedly expand. In the near
future, the use of high technology imaging systems, such as high-speed
CTA, magnetic resonance angiography, smaller and higher frequency
transesophageal ultrasound probes, and intravascular ultrasound probes
will hopefully advance the resolution and details of the small arteries
of avian patients and improve the sensitivity available for diagnosing
vascular pathologic processes.